Colony Collapse Disorder: An Introduction

Shortly after I graduated high school, commercial apiaries started to report massive losses of honeybees. Honeybees are probably the most economically valuable insects in the world, and are responsible for pollinating most of the food we eat. Here in the United States there’s an entire industry built up behind honeybees, with most US honeybees being transported to California to pollinate almonds at some point in the year.Unfortunately there are a lot of wrong-headed things out there in the press. One common idea I see spread through facebook meme, such as the image to the left, is that biotech crops are responsible for killing the bees. This is a hypothesis that’s been pretty thoroughly researched in a variety of ways. Industry data very strongly indicates this is not the case: a recent meta analysis performed by Monsanto published in PLOS ONE reviewed experiments done by a wide variety of researchers and concluded that there were no effects on survival of bees on Bt crops. Academic research is consistent with the industry data, from a 2005 review on the nontarget effects of Bt crops in the Annual Review of Entomology:

Neither Bt cotton nor Bt maize requires bees for pollination, but cotton nectar is attractive to them and produces a useful honey. Maize pollen may be collected when other pollen sources are scarce. Pre-release honey bee biosafety tests have been conducted for each Bt crop registered in the United States, including Cry9C maize and Cry3A potatoes. Each test involved feeding bee larvae and sometimes adults with purified Cry proteins in sucrose solutions at concentrations that greatly exceeded those recorded from the pollen or nectar of the GM plants in question. In each case, no effects were observed. The rationale for requiring larval and not adult bee tests is questionable, because adult bees ingest considerable quantities of pollen in their first few days post emergence. Larvae, particularly later instars, also consume pollen along with jelly secreted by nurse adult bees, but only recently have there been attempts to quantify pollen ingestion by individual larvae. Other studies with bees fed purified Bt proteins, or pollen from Bt plants, or bees allowed to forage on Bt plants in the field have confirmed the lack of effects noted by the U.S. Environmental Protection Agency (EPA). Post-release monitoring programs are now underway to assess impacts of North American GM crops on pollinators under commercial field conditions.

Admittedly, there could be better data on this subject. For instance some of the research that’s been done has been done without some essential controls, like this German group which fed honeybee larvae a mixture of Bt pollen without determining that active Bt proteins were present in the pollen. The data, however, is generally against the idea that Bt crops harm bees.

The failure of foraging bees to return to their hives has led many people to suggest that a link exists between CCD and the behavioral disruptions observed with sublethal exposure to neonicotinoid insecticides. As of yet, no single insecticide or combination of insecticides have been linked to CCD, though many chemicals have been found in hives. Researchers that compared gene expression in honey bees from healthy colonies and from collapsed colonies found no link between expression of genes that code for proteins associated with the detoxification of insecticides and collapsed colonies. This suggests that insecticide exposure, whether to neonicotinoids or another class, is not a primary factor in CCD….
…While neonicotinoids and other agrochemicals do not appear to be the direct cause of CCD, they may be a contributing factor to already stressed colonies. It is increasingly important that future studies focus on interactions of multiple factors suspected of contributing to CCD.

My favorite TV show, Doctor Who even jumped in on the commotion by claiming that the bees had returned home to an alien planet:

There aren’t a lot of easy answers on the topic, and pesticides are probably one of the better ideas being tossed around in the popular media. There are some good reasons to think that some pesticides, especially neonicotinoids, may be a big contributing factor. However, the losses began well after crops expressing Bt proteins were adopted and a very long time after neonicotinoids were adopted so these have never struck me as likely cuplrits. While the Doctor Who episode featured the disappearance as a mostly tongue-in-cheek thing, religious fanatics have suggested that this was a sign of the apocalypse. Cellphones have also been another popular crackpot theory. So it’s unlikely that these are factors in colony collapse.
Personally, I wish I could say definitively that GMOs or neonicotinoids were responsible for Colony Collapse Disorder because then I could say that we knew why the bees are disappearing. Instead, there are a lot more factors to consider. While it would be a simple task to fill Biofortified with an unfruitful discussion of what colony collapse isn’t, I think it would be a much better idea to discuss what colony collapse disorder is, talk about some of the factors involved in the decline of honeybees,and engage in follow-up discussions in the comments.
I’m going to break this article into 5 sections:

History of Beekeeping

Honeybee Biology and Apid Ecology

Parasites Pathogens and Pesticides

Nutrition

The Big Picture

While I’d like to discuss each in detail, the list is going to be very incomplete. For each section, I’m going to give a snapshot: I just want readers to be aware that this is a huge area of research.

History of Beekeeping

Earler, I said that I didn’t think Bt crops or neonicotinoid insecticides were direct causes because they were relatively new things. There are reasons for this. The first thing you need to realize when reading up on this subject is that we’ve been keeping bees for awhile. About 15,000 years ago, some enterprising caveman discovered that bees stockpiled delicious honey and we began braving sheer cliffs and angry insects to collect this honey. Awhile later, another enterprising individual discovered that you could build boxes to keep bees in and by about 5,000 years ago the very basic foundations of modern beekeeping were laid out. If one of those ancient beekeepers were kidnapped by The Doctor and transported to a modern apairy, they probably wouldn’t be completely lost. The materials have changed, but the methods of beekeeping haven’t really changed all that much.
For as long as we’ve been keeping good records, we’ve recorded losses. One of the articles announcing the Colony Collapse problem appeared in PLOS Biology in 2007, and described these ancient losses in quite a bit of detail:

Some winter losses are normal, and because the proportion of colonies dying varies enormously from year to year, it is difficult to say when a crisis is occurring and when losses are part of the normal continuum. What is clear is that about one year in ten, apiarists suffer unusually heavy colony losses. This has been going on for a long time. In Ireland, there was a “great mortality of bees” in 950, and again in 992 and 1443. One of the most famous events was in the spring of 1906, when most beekeepers on the Isle of Wight (United Kingdom) lost all of their colonies. American beekeepers also suffer heavy losses periodically. In 1903, in the Cache valley of Utah, 2000 colonies were lost to a mysterious “disappearing disease” following a “hard winter and cold spring”. More recently, there was an incident in 1995 in which Pennsylvania beekeepers lost 53% of colonies.
Often terms such as “disappearing disease” or “spring dwindling” are used to describe the syndrome in which large numbers of colonies die in spring due to a lack of adult bees. However in 2007, some beekeepers experienced 80–100% losses. This is certainly the extreme end of a continuum, so perhaps there is indeed some new factor in play.

Furthermore, the original USDA action plan reviews some other serious threats to beekeeping that happened at the same time. While worrying is a legitimate reaction, I’m not entirely convinced that this is a new phenomenon. It’s entirely possible that similar things have happened before. However, there are a few more confounding factors which prevent us from being able to say that the same problems are coming around again. There are new things around, like neonicotinoids and pyrethroids (specifically fluvalinate) which weren’t around then and could be contributing today. There are also other new things, like a shrinking environment, constant travel and increased global spread of disease organisms, which are probably contributing factors. However, given the fact that similar things have happened in the past it’s unlikely that we’re dealing with a completely new phenomenon.

Honeybee Biology and Apid Ecology

Honeybees aren’t your average insect, and there are many quirks of their biology that make them unusual if you compare them to more common livestock like sheep or pigs. A lot of these factors make them more susceptible to parasites and pathogens. Honeybees are weird in that they’re difficult to think of as a collection of multiple organisms, but in my opinion, are more accurately described as a superorganism. Superorganisms are a collection of entities that function as a single organism. While honeybee colonies consist of thousands of individuals, the colony functions as a single creature.
Honeybees are very highly evolved eusocial organisms with a strict division of labor, both in terms of reproduction and everyday nest maintenance. Unlike humans and ants, honeybees need more than a male and a female to found a nest. The colony begins when a drone mates with a virgin queen, and after she returns a big chunk of the colony splits off to form a new colony. The queen is incapable of raising larvae by herself, and if you were to put a mated queen in a beehive there would be no colony. Instead, she needs workers to build wax combs in which to lay her eggs. These workers have their own division of labor based on age: young workers clean the nest and tend the young, middle age workers forage and older workers forage and defend the colony. To reproduce, the bees need all these groups. They need drones and queens to reproduce, and the workers to do the work. Without all of these working in unison, there is no bee colony.
These social roles are very important, and a large part of honeybee immunity revolves around social roles. Bees keep the colonies quite clean, and even work together to seal the hive from invaders with propolis. Besides sealing the colony, propolis also has antimicrobial properties. It’s not the cure for cancer, but it likely stops the spread of bacteria and viruses. While bees within colonies tend to stick to themselves, there are circumstances where stranded workers may enter another hive… especially if their home colony is suddenly transported out of foraging range. During later times of the year, stronger colonies may raid weaker colonies.
With this in mind, the 2007 USDA action plan defines CCD thusly:

Symptoms of CCD include: (i) sudden loss of the colony’s adult bee population with very few bees found near the dead colonies; (ii) several frames with healthy, capped brood with low levels of parasitic mites, indicating that colonies were relatively strong shortly before the loss of adult bees and that the losses cannot be attributed to a recent infestation of mites; (iii) food reserves that have not been robbed, despite active colonies in the same area, suggesting avoidance of the dead colony by other bees; (iv) minimal evidence of wax moth or small hive beetle damage; and (v) a laying queen often present with a small cluster of newly emerged attendants

We’ll discuss those parasites later.
**One problem that I see consistently in online discussions of Colony Collapse Disorder is that many assume that any loss of bee colonies is the same thing as CCD. There are many reasons a honeybee colony can die, and the definition of CCD above eliminates some of the other possibilities. For example, under the second symptom (ii) there must be low levels of Varroa mites which means that the colonies aren’t killed by Varroa mites. Later definitions also remove colonies with damaging levels of Nosema. Pesticide poisoning also results in large numbers of dead bees around the hive, so direct pesticide poisoning does not match up with these symptoms.
While it’s tempting to assume that these symptoms are explained by only the older workers being afflicted, I would caution against that interpretation because it can be explained equally well by a slow-acting agent acquired as larvae that finally kills the bees well after they’ve emerged as adults. The fact that only newly emerged adult bees are still present means that newly emerged adult bees are still present.
The other thing that you need to realize is that we get a lot of pollination services from native bees, and those native bees we rely on for pollination are in trouble as well. In fact invertebrates as a group aren’t doing too well, but bees seem to be particularly hard hit. Ecosystem fragmentation and loss of plant diversity are definitely major contributors, but cross-contamination of pathogens between native and our introduced honeybees is probably a contributing factor. In other words, we’re losing vital pollinators on two fronts, and it’s too early to know for sure if the two events are related.

Parasites, Pathogens and Pesticides

Some of these guys we’ve already mentioned, but have yet to discuss in detail. Honeybees, like virtually every other organism on the planet, have their own set of parasites and pathogens which can wreak havoc on bee colonies. Some will immunosuppress the adults, others weaken the entire colony, while others target larvae. The list of pathogens is quite long, and some are bigger problems in some parts of the world and in some parts of the country. I could easily devote an entire post to their biology, but here are just four along with the problems they cause:

Deformed Wing Virus (DWV) is a virus which infects honeybees, and is spread among the workers in a colony. Under certain circumstances, which I’ll describe later, the virus can replicate out of control and cause damage in honeybee colonies. The damage results from lots of honeybees having deformed body parts, and stunted wings. A good chunk of these bees die after soon after they emerge.

Nosemaare single celled fungal parasites. They inject their cell’s cytoplasm into the intestinal cell of the bee and replicate rapidly. The parasite is spread through the feces, and often you can tell if a colony has a Nosema infection by looking for larger than normal amounts of feces around the outside of the hive. Infected bees are puffy and white, and have trouble absorbing nutrients from their food. Infected bees are quite easy to tell apart from noninfected bees.

Paralytic viruses is a broad category that includes several different viruses, among them Acute Paralysis Virus and Israeli Acute Paralysis Virus. These viruses do pretty much exactly what it sounds like, they slowly render the bee immobile and unable to fly. The role of these viruses is controversial because some research indicates that they’re involved, while other groups downplay their role.

Varroa destructoris a parasitic mite that’s closely related to ticks. They attach to the outside of honeybee adults and larvae and suck their hemolymph, knocking their immune system out to facilitate this process. V. destructor also vectors viral pathogens. The damage from V. destructor infestation is both from transmission of disease and from removal of hemolymph.

These are just four pathogens that are major problems in honeybees, but they’re not neccessarily culprits in the Colony Collapse problem. There are also insects that play a role in weakening honeybee colonies. Hive beetles will burrow through honeycomb, consuming pollen and bee larvae. Waxworms are caterpillar larvae which burrow through frames of beeswax that are in storage. While these organisms generally steer clear of hives implicated in CCD, it’s possible they could still play a role by tracking pathogens into colonies.
Bees fight these pathogens off in three ways. First, as already mentioned, they line most of their colonies with propolis which has antimicrobial properties. Second, they practice a form of socialized medicine where they will expel diseased larvae and adults from the colony. They can also practice a so-called ‘behavioral fever’ where the bees vibrate their bodies to overheat intruders. Some bees have also learned to use this against predators, as shown in the video at the bottom of this section.
A third form of defense is the bee’s immune system. They have a full compliment of weapons at their disposal, from antibiotic proteins that form holes in bacterial cells and blow them up, to RNAinterference that destroys nucleic acide sequences of viruses, to hemocytes that encapsulate invaders. However, they tend to rely more on sanitation than their immune system. One thing worth mentioning isn’t what they have, but what they lack. The husbandry of other livestock has certainly benefited from the fact that they can be used as models for humans, but bees aren’t so lucky. Honeybees are insects, and insects lack an antibody production system. Because they don’t produce antibodies, they can’t be vaccinated*.
Bees are exposed to quite a few pesticides, believe it or not. These not only include pesticides that they’re exposed to while foraging (i.e. those neionicotinoids), but also pesticides that they’re exposed to in order to combat V. destructor. There are sophisticated sampling methods to sample for V. destructor and there are damage thresholds that have been set. Thus, V. destructor can be managed in an Integrated Pest Management (IPM) setting.
Fluvalinate is a synthetic pyrethroid that’s more toxic to mites than to bees, and this is used to control V. destructor in bee colonies. Organophosphate insecticides, namely Coumaphos, are used when pyrethroid insecticides fail because of resistance. When frames are stored, waxworms are sometimes controlled with napthalene, the active ingredient in mothballs.

Nutrition and Stress

A lot of people imagine aparies as places that are surrounded by miles of quiet little meadows like what you see on TV, but sadly this is not the case. Honeybees are likely impacted by the fragmentation of habitat just like native bees, and their diets are often supplemented by nectar substitutes like high fructose corn syrup. While high sugar diets in humans contribute to obesity by increasing calories, the diets of bees consist largely of sugary liquids like nectar. The problem is that wild nectar contains lots of sugar in addition to other things like amino acids that are lacking in HFCS, and other substitutes aren’t economically viable.
Furthermore, bees are exposed to a lot of variable conditions when they travel. They need a high diversity of pollen because pollen can vary widely in it’s nutritional composition. When the honeybees are loaded onto trucks and transported cross-country it’s questionable whether they’d be exposed to the types of pollen that are, nutritionally speaking, best for them.These would presumably be in protein rich pollen substitutes, but I’m unaware of any studies that have evaluated whether these will nourish well enough to support an immune response.

The Big Picture

Pathogens, pesticides and all the other factors I mentioned above do not exist in a vacuum. Instead, everything interacts with everything else. Pathogens co-infect bees in the field and a lot of the research that’s underway is aimed at looking at the bee pathogens which are correlated with Colony Collapse. Unfortunately, there are no pathogens which are correlated with Colony Collapse. There are no pesticides which are exclusively connected with Colony Collapse, either. There are also no genes which are consistently upregulated in Colony Collapse colonies. Instead, it looks like there are a bunch of smaller incidents which involve a lot of factors acting in unison.
The reason why there’s a lot of focus on diseases in CCD research is because CCD bees tend to have higher numbers of bee pathogens, and lots of different pathogens. The problem, however, is that there are no diseases that are exclusively associated with CCD. Furthermore, a lot of the pathogens that are in healthy colonies are also found in CCD colonies. Researchers are just starting to understand these interactions. A recent PLOS ONE paper shows how complicated these interactions can be. In the figure below, the circles represent different pathogens, and the black lines represent correlations. The bigger the circle, the greater the proportion of bees in the colonies that are infected. The thicker the lines, the stronger the correlations between pathogens.
Some pathogens, like Nosema apis (N. apis), Kashmir Bee Virus (KBV), and Acute Bee Paralysis Virus (ABPV) are detected more commonly in collapsing colonies which is denoted by the size of the circles. In collapsing colonies, how often different pairs of pathogens are detected in the colonies are shown by the thickness of the lines. Unfortunately, at this time, we’re not sure whether these pathogens are causing the collapse of the colonies or if they’re there because the colonies are collapsing.
All of these pathogens have been shown to be able to kill bee colonies, but whether they’re actually killing the colonies is hard to determine. There are instances where some of these pathogens, like Deformed Wing Virus (DWV) can be present but not cause symptoms and there are conditions which cause the same pathogens to become very problematic.
One such interaction is between Varroa destructor and DWV. To ensure a meal, the mites have to immunosuppress their hosts. In other animals, this often creates openings that allow other pathogens to establish. Nazzi et. al 2012 did a pretty good series of tests looking at how infestation of V. destructor changes infection by Deformed Wing Virus. They found that by artificially infesting bees infected with DWV with V. destructor, they could get the number of DWV genome copies to increase by quite a bit. Then, they looked at expression of an immune factor connected to the NF-KB pathway, Dorsal, as a product of viral infection and found that only viral infection but not mite feeding caused a decrease in the production of RNA that codes for this protein. Artificial silencing of Dorsal resulted in an increase of DWV reproduction. As more mites feed on the bees, the more susceptible the bees become to DWV. Because the viruses are able to replicate easier, they’re able to better drive down the transcription of factors that play a role in defense against viruses. The results from their study pretty strongly imply that feeding of the mites causes a loop that results in DWV replicating out of control, and higher levels of DWV cause the bees to die at a faster rate. Because some factors involved in antiviral immunity are downregulated, it also implies that bees that are both infested with V. destructor and infected with DWV are more susceptible to infection by other pathogens.
The V. destructor-DWV interaction is worth mentioning, not because it’s important for CCD but because it describes the type of research that needs to be done. V. destructor is frequently sampled for and relatively easy to detect, which means that this parasite is easily controlled. Similar interactions between honeybee pathogens may go undetected, and V. destructor is present at some level in most colonies. While V. destructor may be absent from collapsing colonies, the diseases it vectors are still present and we don’t understand how these diseases interact.
Finally, not all honeybee diseases are well studied. There are some organisms, notably Malpighamobea mellificae, which cause diseases in honeybees but haven’t been studied since the 1960s. M. mellificae replicates in the bee’s Malpighian tubules (kind of like their kidneys) and keep these from functioning properly. They can cause problems in beehives, especially around springtime when the bees are recovering from hard winters. The infected bees get a form of dysentary, and often flee the colony in a manner similar to Collapsing hives. Since there’s no research on the pathogen, it’s unclear if this pathogen plays any role in Colony Collapse (Evans and Schwarz, 2011).

Conclusions

There are a lot of factors involved in colony collapse disorder, and it’s unlikely that there is ‘One True Cause of Colony Collapse’. There are a lot of things that correlate with the symptoms and timelines, but we have to start to separate these. Above, I’ve shown a lot of things that correlate with collapsing colonies… but at the same time, so did my high-school graduation. A correlation can shed light on some details of the problem, but this isn’t the same thing as causation. We know that similar incidents have happened before, but they were a lot more localized than the current set of events. Pesticides, pathogens and environmental factors are likely to be involved but we’ve really got no idea what role these factors play at the current time. There’s good progress being made, but it’s still too early to know why it’s happening this time around.
While we might not know exactly why honeybee colonies are dying, there are a lot of good entomologists trying to figure out what factors are involved in Colony Collapse. The stuff I’ve described above is merely a snapshot of a small subset of interactions which entomologists have to dig through to get to the heart of the problem. Throughout this entire piece, I’ve tried to stick to open-access literature so interested readers can have access to good information on this stuff. If you’re interested in further reading, there are a variety of institutions which have good information. The Xerces Society does a lot of great work on studying the native bees. The USDA has a great webpage on Colony Collapse Disorder and puts out annual open-access reports on what progress has been made on CCD over the past few years..
* The use of the term ‘vaccination’ is controversial within insect immunology because some (including myself) think it implies antibody production. Instead of producing antibodies, insects rely on proteins that detect broad classes of pathogens. They can modify how specific and sensitive their immune response is by upregulating certian components these after exposure, and in some cases ‘store’ bits of double-stranded RNA. There’s research ongoing to determine if exposure to bits of pathogen could be used as a prophylactic measure in the way we use vaccines.
**This paragraph was added by edit on 3/14/2013 after my first comment below.

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22 comments

Excellent post and very well explained, thanks!
There are a couple of pieces of CCD information that I’ve struggled to find in recent years and wondered if you could recommend any papers/resources/reports that could provide answers.
1- Is there a record of annual reported CCD losses around the world? It’s difficult to know whether it is still an increasing problem or if incidences have levelled/reduced since 2006.
2- Is there a resource that shows which regions around the globe have been affected by CCD? It’s surprisingly hard to find this information. Most websites focus on the US.
Thanks in advance if you could help a layman like myself further understand this complex and interesting area.

Unfortunately, despite the enormous effort you have put into this, you are sadly wrong.
I suggest you read the Buglife Report here:http://www.buglife.org.uk/Resources/Buglife/revised%20neonics%20report.pdf
“The impact of neonicotinoid
insecticides on bumblebees,
Honey bees and other non-
target invertebrates
(revised version)
Vicky Kindemba
2009 ”
This is a meta-analysis of over 50 peer reviewed studies going back as far as 2000AD , when the French Government banned neonicotinoids on sunflowers, oilseed rape and maize – after 1,000,000 French bee colonies were lost, following the introduction of Bayer’s imidacloprid based systemic pesticide ‘Gaucho’ on sunflowers.
Buglife also issued an updated review, which classified more than 50 peer reviewed papers into one of three classes:
1. The study assigned neonics the major role in colony collapse
2. The study concluded neonics played no role in CCD
3. The study came to no conclusion either way.
Six papers fell into category 3. (we just don’t know)
Two papers (4%) fell into category 2 (neonics are innocent)
Forty four papers (96%) fell into category 1 (neonics cause the global pandemic of bee deaths)
Guess which two papers were funded by the pesticide industry?
Guess which 44 papers were funded by governments or independent sources?
If you send me an email I will gladly send you the key studies/
I write as a beekeeper of 18 years experience who has just lost 80% of my colonies during this current winter – and it was not down to varroa or viruses. I live in an area of intense oilseed rape cultivation where the entire landscape for 20 miles radius is dominated by neonic treated OSR/

Graham , sorry to hear of your loss. That is a devistating feeling. My bees died this winter as well, but it was definitely not CCD. Can you definitely attribute your loss to CCD? We’re all the bees gone? Did you observe dead bees? Larvae? Dead hives != CCD, but the association is often made.
Also, explain low CCD rates in Austrailia, which regularly uses neonics.
Likewise, explain CCD in France, which has banned neonic use for many years (longer than the typical half life).
BTW, the commercial beeks here often seek out canola and rape seed fields for their hives (yes, the fields/seeds are treated). They have no problems out of the ordinary.

Andre,
That gets to the heart of the issue that I’d like to address with this post.
Bees die during winter for a number of reasons. Varroa/DWV and Nosema are big reasons. Sometimes the ventilation’s not good in the overwintering building, and the bees die from CO2 buildup. Stuff like this accounts for about 2/3rds of losses of US bee colonies. Colony Collapse Disorder is a very specific syndrome, whose symptoms are listed above. This accounts for about the other third.
There have been researchers who have looked at the pesticides found in bee colonies diagnosed with CCD, as well as expression of detoxification genes in bees from colonies diagnosed with CCD. Neither of these revealed any correlations with pesticides.
Now the problem is that European bee colonies are in trouble as well, and these trends have continued in areas that have banned neonics. Only recently have European researchers started to standardize case definitions with the American CCD case definition (see link above).
So, that still leaves us on Square One. Neonics have troubling sublethal effects which could affect honeybee health, and they seem to interact with some parasites. But, we don’t know the full extent of these effects.
The big problem with Neonics in Europe is that they were worse for bees than preliminary research indicated. Folks are trying to figure out exactly how much worse they were.
Native bee losses are another monster, as there are a lot of factors that are different between honeybees. Diet, pesticide exposure, stress…all of these would be very different in important ways.
I’m really trying to avoid link-dumping here, so I’m limiting myself to one or two papers per reply. Here are the papers cited in the Xerces report for pesticides and gene expression, with some comments.
Immune and pesticide toxicity gene expression:http://www.pnas.org/content/early/2009/08/21/0906970106.abstract
When this paper was published, it was very controversial because it was published in a high profile journal and didn’t demonstrate any clear patterns in expression of pesticide detox or immune related genes. One problem, however, is that it used microarrays which have some issues associated with them. At the time, this was top-of-the line methodology…but I personally think it needs to be replicated with RNA-Seq.
This paper will give you an idea of how complex the pesticide situation is in honeybee colonies:http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0009754
There are a *lot* of pesticides…literally dozens…found in appreciable concentrations inside honeybee colonies. There are learning defects that have been documented in non-neonic pesticides, and there’s all sorts of synergism that can happen between different pesticide classes. It’s going to be a lot of work to tease this all out, and neonics are only a tiny part of this story.

While the Buglife report correctly shows the high risks neonics present to bees, they do not show a conclusive link to CCD. Considering how sensitive honeybees are to many other pesticides, you could probably draw up a similar document for other classes.

Jonathan,
I’ve been following the CCD data through the USDA reports over the past few years, and these focus mostly on American hives. In Europe, there have been a lot of unexplained bee deaths but only recently have some of these incidents been attributed to CCD. As far as I know, and somebody correct me if I’m wrong, they’re still trying to ascertain how big of a problem CCD is in Europe. We know it’s there…but we don’t know how much.
Here in America, colony losses have been hovering at about 30%/year since 2006 (down to 20% in 2012). About one in three of these was actually attributable to CCD.http://onlinelibrary.wiley.com/doi/10.1111/j.1758-2229.2011.00312.x/abstract
Graham,
As Bill said, CCD is not the same thing as dead bees or dying colonies. CCD is a very specific syndrome which involves a rapid decline of healthy colonies where there is still a queen and some young workers present with few dead bees around the hives, among other things. The differential diagnosis for CCD is listed out above, and has recently been amended to include ‘non-damaging levels of Nosema’ as a part of it.
Saying that neonicotinoids are a high risk to bees is very different than saying that they cause CCD. That neonics aren’t good for bees isn’t up for debate (the Xerces report basically says they aren’t), but what we’re actually debating is whether they cause the list of symptoms above. There have been incidents where bees were poisoned by neonics, and in each case this resulted in large numbers of dead bees in and around the hive.
So…neonic poisoning does not match the symptoms of CCD, and I think I need to edit the post to more bluntly state that CCD is not the same thing as dead bees. They’ve done surveys of pesticides, and none have explicitly been connected with CCD. Sure, neonics can disrupt some of the social aspects of honeybee life…but that doesn’t make them The One True Cause of CCD.
****
Furthermore, the Buglife report Graham White hyperlinked to doesn’t make a single mention of CCD as far as I can tell. I scanned it and they do mention colony losses, but that is *not* the same thing as CCD. I also did a couple word searches (Colony, colony collapse, colony collapse disorder, CCD) to verify this. The report Graham linked to doesn’t contain the text he pasted, and I can’t locate the source for the text via google.
The Buglife report is very similar to the Xerces report, except for the fact that it’s a European thing and not an American thing. That being said, I think it’s odd that a European agency would be trying to sort out the American CCD problem without doing a survey to determine the extent of the CCD problem in Europe. So, I went to their website to try to locate the report.
The portion of the website with the link to the report that Graham linked to states this in reference to neonics in the very first line:
“While this is unlikely to explain Colony Collapse Disorder in the Honey bee, it could be a key contributory factor and may well be part of the cause for widespread declines in wild bee populations. The report also exposes that the current process for approving crop pesticides is inadequate for assessing risks to bees and other wildlife.”http://www.buglife.org.uk/conservation/campaigns/Pesticides+Poisoning+Our+Bees
So, even Buglife does not appear to support a direct CCD-Neonic link. I’m not saying that they’re not involved, but it’s not nearly as simple as “CCD is neonic poisoning”. The jury’s still out as to what extent sublethal levels of neonics can disrupt honeybee social structures in field situations. It’s likely there’s some amount of disruption, but I’ve yet to see a paper that demonstrated that neonics can cause bees to abandon a colony in a manner that replicates CCD.
However, there is always the possibility I’ve missed something. If you want to send me the updated Buglife meta-analysis, Biofortified has a contact button. I’m not going to give a personal E-mail account out online.
Also, please don’t link-dump. If I want to read the original papers, I should be able to locate them through Web of Knowledge. Just send the meta-analysis, please.

Joe, thanks for the writeup. I have a question about bee nutrition. I want to stress that it is a question, not even a suggestion.
All the attempts to connect CCD with GMO agriculture assume some sort of poisoning is the potential cause. But if diminished bee nutrition is a contributing cause, is it possible that the better weed control that GMO herbicide tolerance makes possible has deprived some bees of pollen variety? E.g. if a population of bees was depending on some weeds as a supplemental source of pollen to contribute a nutrient that was deficient in pollen from the dominant local crop, then better weed control could deprive the bees of that variability.

This point has been made about monarch butterflies, too – that herbicide tolerant crops are the cause for lower amounts of weeds. Yes of course that contributes, but I’m thinking there’s lots of other factors as well – such as farm consolidation removing spaces between farms, GPS allowing farmers to spray more precisely (less missed areas) and right up to field edges), and the removal of marginal acres from CRP thanks to high corn prices.

Charles,
I really want to thank you for asking that question, because I have to concede that I did not consider that angle. Changes in agricultural landscapes (particularly in weedy areas) have detrimental impacts on both native bees and honeybees because it reduces the amount of food they have to eat. Better weed control means fewer weeds, fewer weeds means less food, less food means worse nutrition.
When reading up on GMOs and bees, a lot of the things I read from activists focus mostly on Bt crops and assume a more direct role for GMO crops. I clearly had this in mind when I wrote this piece, and perhaps I was a bit myopic.
As Anastasia said, however, there are a lot of landscape changes that result in the reduction of weedy forage. We’ve come a long way, technologically speaking, in the way we manage weeds. More effective herbicides, and herbicide tolerant crops are a part of the new technology. New technology always creates new problems, and advances in how we control for weeds are no different.
So, yes…herbicide tolerant crops play a very small and indirect role in causing this problem. However, there are a lot more facets.

I’ve heard that hives located in inner-city areas do better than ones in the country. Has there been any research on this? And if it is the case does it lend weight to the suspicion that poor food source variety may have a part to play in CCD?

This will probably throw some fuel on the GMO-conspiracy fire… Are there attempts at genetically modifying bees to (1) determine if there are endogenous genes that cause increased or decreased susceptibility to CCD and (2) create resistant strains? I know that question 2 is kind of hard to address without knowing the ultimate cause of CCD but would engineered disease and/or insecticide resistance be a way forward?

Tom,
Unfortunately, as I understand the situation, there are genes we may be able to use to monitor for CCD (as defined above)…but I’m not sure that we know a whole lot about genes that determine susceptibility.
As for insecticide resistance, that’s a much tougher question. The average pollen sample contains a lot of different pesticides which can vary widely according to geographic location. I’m very specific in how I use the term pesticide, and not all of these are *insect*icides. Fungicides and herbicides are also found in pollen samples, and some fungicides are known to interact with insecticides.
I’m not sure that breeding for insecticide resistance is a way forward. Instead, I think we should be a lot more careful about how we apply pesticides when plants are flowering. Even that, though…there’s no way to know what impact that would have.
There are groups that are breeding honeybees to become better at controlling mites for themselves. Since those mites vector a lot of diseases, that would go a long way towards breaking that cycle. Some of the most common insecticides found in honeybee hives are those used to control mites, and that would go a long way towards reducing honeybee stress.

Genetic modification has already been used on the Dengue Fever vectoring mosquito, Aedes aegypti to produce sterile males that disrupt reproduction. It may be possible to do something to incorporate resistance into the honeybee.

This is what the regulators let loose in 2004(see below). It is all based on industry “research”. Since then there has been another failed industry “study” and thousands of acute and chronically affected honeybee colonies dieing. 70 % of the 100’s of dead bee samples taken by gov. inspectors tested + for Clothianidin. In the meantime the pesticide companies have made billions of dollars on this group of chemicals.
Regulatory Note REG2004-06
Clothianidin
2. Poncho 600
Seed Treatment Insecticide
4. 6.0 Effects on non-target species
1. 6.2.2 Terrestrial organisms
6.2.2.1 Non-target terrestrial invertebrates
Clothianidin is very highly toxic to honey bees, with a 48-hour acute oral LD50 of 0.00368 μg a.i./bee (= 3.68 ng a.i./bee). The transformation products TMG, MNG, TZMU and TZNG, however, were of relatively lower toxicity to the honey bees. Field or semi- field studies conducted in Sweden, the United Kingdom, France and Germany as well as in Ontario (Canada) and Minnesota (United States) indicated that there were no significant impacts on honey bees compared with the controls. All of the field/semi-field studies, however, were found to be deficient in design and conduct of the studies and were, therefore, considered as supplemental information only. Moreover, the results of most of the studies indicated that residues of clothianidin, when used as a canola (rapeseed) seed treatment insecticide, were expressed in pollen and nectar of the crop plants (or collected from foraging bees) in concentrations which exceed the measured
Regulatory Note – REG2004-06 Page 31
6.2.2.2
acute oral LD50 to the honey bee. The effects on honey bee hives from chronic/long-term exposure to clothianidin residues are unknown. It should also be noted that clothianidin is very persistent in soil, with high carry-over of residues to the next growing season. Clothianidin is also mobile in soil.
Given the foregoing, the risk that clothianidin seed treatment may pose to honey bees and other pollinators cannot be fully assessed, owing to the lack of sufficient information and data. Clothianidin may pose a risk to honey bees and other pollinators, if exposure occurs via pollen and nectar of crop plants grown from treated seeds.

Old Drone,
The Xerces report I linked to in the original post discusses all of this. Neonics are very likely bad for bees. Again, not exactly a controversial statement…and something I said in the original post.
Furthermore, as I said in my original post, Colony Collapse Disorder and dead bees are not synonymous with one another. CCD is largely characterized by hive abandonment, whereas the study you’re talking about seems to be talking about dead bees. This very strongly indicates the condition I am talking about (CCD) and the condition YOU are talking about (acute neonicotinoid poisoning) are completely different.
If you would link me to the exact study you’re talking about (which I’m not going to dig up), that would be the best way to facilitate further conversation.

Thank you Joe, for having to point this out yet again. Dead bees do not automatically = CCD. Their equivalence is another one of those zombie memes that will never go away 🙁
On another topic, do you know of many studies regarding Amygdalin (from almond) levels in hives and bees? I am familiar with the London-Shafir (2003) work, but was wondering if this had been looked at more.http://link.springer.com/article/10.1007/s00606-003-0272-y#page-1

Does anyone have links to field studies that measure neonic levels found in pollen for different seed treated crops? Given how little long-term above-ground insect protection these seed treatments give us I’m curious to what extent the pollen of a treated crop could be an issue.

The European Commission has requested the European Food Safety Authority to assess the risks associated with the use of clothianidin, imidacloprid and thiamethoxam.
EFSA delivered its opinions on 16 January 2013. Available starting at:http://www.efsa.europa.eu/en/press/news/130116.htm?utm_medium=infocus&utm_source=homepage&utm_campaign=beehealth
This gave rise to a lot of dysinformation, starting by EFSA’s own communication team which, to set out the most grotesque here, produced a press release with different keypoints in different languages. For an analysis (in French):http://www.imposteurs.org/article-neonicotinoides-scandale-mediatique-et-politique-sur-fond-d-expertise-de-l-efsa-par-wackes-seppi-115227070.html
The European Commission in turn rang the alarm bell and proposed a « temporary » (I am putting quotation marks to indicate that the « temporary », if accepted, will of course be permanent) two-year ban on the major uses of the three neonics in order, the Commission claims, to get evidence on their role in bee losses (pretty stupid approach as there would be no checks…).
So far, the proposal has failed. A new attempt to gather a majority for an amended proposal should be made shortly.
The United Kingdom Government is one of the few that advocates science-based policies rather than policy-based « science ». It produced « An assessment of key evidence about Neonicotinoids and bees »:https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/181841/pb13937-neonicotinoid-bees-20130326.pdf.pdf
There was also a field trial which led to an article in Nature :http://blogs.nature.com/news/2013/03/uk-study-casts-doubt-on-insecticide-link-to-bee-declines.html
Full trial report:http://www.fera.defra.gov.uk/scienceResearch/scienceCapabilities/chemicalsEnvironment/documents/reportPS2371Mar13.pdf
The gist (from Nature):
« Now, a field trial run by FERA [the UK Food and Environment Research Agency], based in Sand Hutton, has failed to find any “clear consistent relationship” between neonicotinoid residues and the size of bumblebee colonies or the number of new queens they produce. “The absence of these effects is reassuring but not definitive,” says the FERA study, which involved assessing the health of colonies near crops grown from seeds that were treated with clothianidin and imidacloprid. »
Needless to say that the issue of neonics and bees is extremely politicised in Europe. The question arises whether safety experts in Europe are still able to produce objective assessments, against all sorts of pressures – by so-called NGOs, media, politicians. My answer is: no!
The neonic reports testify to this. The EFSA spin doctors wrote: « EFSA scientists have identified a number of risks posed to bees by three neonicotinoid insecticides… ». Yet the reports include a final table which summarises the monitoring reports from member States, i.e. the feedback from field observations. The overall picture is that the situation is not as bleak as claimed. Moreover, the table distinguishes between two situations: « risk identified » (whatever that may mean) and, as alternative, « assessment not finalised » (which could mean: still tracking the evidence of risk).
In France (one of the leaders for the ban), thiamethoxam was used over half the oilseed rape area in 2011/2012. There were no complaints from beekeepers in general nor from one of their associations which is extremely vocal on the issue (it behaves in fact like a subsidiary of the anticapitalist movement). How was this translated in the EFSA table? The French did not provide any feedback!

Andre…please re-read what I have written.
Neonics are potentially bad for bees. I’ve mentioned this at least three times now, one of these times being in my original post.
Neonics can potentially cause hive abandonment, but so can pyrethroids and high amounts of CO2. Hive abandonment is a general response. Other pathogens, including IAPV, can also potentially cause CCD-like symptoms. So, nobody has a handle on what actually causes CCD and the relation of any of these to CCD is uncertian.
The papers you’ve posted here all deal with what happens to bees when they’ve been exposed to neonics, and from the brief scan I did none actually looked at neonic residues in CCD hives.
There are researchers who have looked at pesticide residues in hives. They have found lots of different pesticides (and not just insecticides), which clouds the issue of what pesticides are doing to bees. They did find neonicotinoids, but they were in very low concentrations and in a very small percentage of the hives.
In CCD hives, the only pesticides which occur in higher amounts are largely miticides. Not neonicotinoids. So, no correlation there. As I pointed out earlier there’s also little correlation in the timeline. There are also massive hive losses in areas where neonics aren’t used, but nobody knows if this is CCD or not.
This issue is far more complex than the papers you’ve posted let on, and there’s an entire world of literature you’ve systematically ignored. I’m tempted to post references again, but this is at least the third time I’ve discussed these papers in this thread. Posting them again would simply be redundant. I refer you to my above posts which discuss the Xerces white paper, and the Pettis PLOS ONE paper.
In other words the papers you have posted here do not support the conclusions you have drawn from them. They are discussing another issue entirely. This is something I basically said in the first paragraph of the original post, and something I flat-out said in multiple previous comments.
Please re-read the post.
Bill,
I am familiar with amygdalin as a cyanogenic glycoside, but I know very little about how it affects honeybees. So, I did a quick search on Web of Knowledge to see if it had been dealt with.
There’s an article in the American Bee Journal which suggests that amygdalin could be potentially harmful to the bees if consumed for more than a week…but they say this is an area where more research is needed.
So…I don’t know that it’s been looked into.

Joe,
I was basically reporting about the situation in Europe. No criticism nor challenging of your post.
The key message is that, with respect to bees and pesticides, particularly neonics, science has left the realm of science to become politicised.